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e  Development  of  Magnolia 

\  :,  i?  and  Liriodendron 

yv\  3 

Including  a  Discussion  of  the  Primitiveness 
of  the  Magnoliaceae 


A  DISSERTATION 

SUBMITTED  TO  THE  BOARD  OF  UNIVERSITY  STUDIES  OF  THE  JOHNS  HOPKINS 
UNIVERSITY,  IN  CONFORMITY  WITH  THE  REQUIREMENTS  FOR 
THE  DEGREE  OF  DOCTOR  OF  PHILOSOPHY 


By 


WILLIS  EDGAR  MANEVAL 


1912 


BIOLOGY 


V 


■  ;Sv,  -  fcgp.rjj 

fLi  ''-'*?  *  -  '  .  r  1 


d 


Botanical  Gazette 

JANUARY  iq  14 

THE  DEVELOPMENT  OF  MAGNOLIA  AND  LIRIODEN- 
DRON,  INCLUDING  A  DISCUSSION  OF  THE 
PRIMITIVENESS  OF  THE  MAGNOLIACEAE1 

Willis  Edgar  Maneval 
(with  PLATES  i-iii) 

The  recently  announced  theories  of  Arber  and  Parkin, 
especially  as  developed  in  their  paper  “On  the  origin  of  angio- 
sperms”  (2),  make  it  desirable  that  more  detailed  work  be  done 
on  the  Magnoliaceae  and  related  groups.  Besides,  as  the  embryo 
sac  of  only  one  species  of  the  Magnoliaceae,  Drimys  Winteri  (29), 
has  ever  been  studied,  it  seemed  probable  that  an  investigation 
of  other  genera  of  this  family,  from  this  point  of  view,  might  be 
of  value  in  several  ways,  but  especially  in  furnishing  either  positive 
or  negative  evidence  concerning  the  primitiveness  of  this  family. 

In  the  present  study  of  Magnolia  virginiana  L.  and  Liriodendron 
TulipiferaL,.  two  objects  have  been  kept  in  mind:  (1)  the  determina¬ 
tion  of  the  course  of  development  of  the  sporogenous  tissues  and 
of  the  mature  gametophytes,  and  also  the  examination  of  certain 
points  concerning  the  gross  structure  and  anatomy  of  these  forms; 
(2)  a  consideration  of  the  primitiveness  of  the  Magnoliaceae  on 
the  basis  of  the  evidence  gained  by  such  investigation,  and  of 
present  prevailing  theories  respecting  the  origin  of  angiosperms. 

The  collection  of  material  was  begun  in  December  of  1910  and 
was  continued  at  intervals  of  generally  two  or  three  weeks  until 

1  Contribution  from  the  Botanical  Laboratory  of  the  Johns  Hopkins  University, 
no.  34. 


HATBWl 

HISTORY 

UBBARY 


NUM 


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THE 


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D 


VOLUME  LVII 


A: 


I 


2 


BOTANICAL  GAZETTE 


[JANUARY 


September  1911.  Material  for  the  study  of  Liriodendron  was 
obtained  at  Homewood,  the  new  site  of  the  Johns  Hopkins  Uni¬ 
versity,  and  that  for  Magnolia  in  a  swampy  region  at  Glen  Burnie, 
Maryland,  a  typical  habitat  for  the  so-called  swamp  magnolia. 
Most  satisfactory  results  were  obtained  by  using  a  chromacetic  solu¬ 
tion  for  fixing,  although  acetic  alcohol  worked  well  also.  The  prin¬ 
cipal  stains  used  for  sporogenous  tissues  and  young  embryo  sacs 
were  iron-hematoxylin  and  orange  G;  and  for  older  sacs  safranin 
and  Delafield’s  hematoxylin,  or  for  embryos  hematoxylin  alone. 

The  writer  is  greatly  indebted  to  Professor  Duncan  S.  Johnson, 
and  desires  to  express  thanks  for  many  suggestions  and  much 
helpful  criticism  during  the  progress  of  the  work. 

As  the  course  of  development  is  very  similar  in  Magnolia  and 
Liriodendron ,  in  the  following  description  attention  will  be  directed 
mainly  to  the  former,  differences  between  the  two  species  being 
pointed  out  where  they  occur. 

The  stamens  of  Magnolia  and  Liriodendron  have  elongated 
anthers  on  short  filaments,  the  connectives  extending  beyond  the 
anthers.  The  anthers  contain  four  locules,  with  walls  of  3  or  4 
layers  of  cells,  and  dehisce  longitudinally.  In  Magnolia  the  spo¬ 
rogenous  tissue  in  the  stamens  is  already  differentiated  early  in 
December  (fig.  15),  and  in  Liriodendron  early  in  January.  Little 
change  occurs  in  this  tissue  until  March,  when  the  sporogenous  cells 
enlarge  considerably  and  divide.  The  nuclei  of  the  microspore 
mother  cells  are  found  in  synapsis  from  April  20  to  May  1  (fig.  16). 
The  first  mitosis  in  both  species  usually  occurs  during  the  first  week 
in  May  (fig.  2),  and  tetrads  are  developed  by  the  simultaneous 
method  about  May  10  (fig.  18). 

After  the  first  and  second  mitosis  of  the  nuclei  of  the  micro¬ 
spore  mother  cells  the  number  of  chromosomes  is  19  (figs.  3  and  19). 
The  actual  number  in  the  microspore  mother  cells,  or  in  the  vegeta¬ 
tive  tissues,  was  not  determined,  but  is  much  greater  than  19; 
therefore,  as  the  usual  heterotypic  division  occurs  in  the  microspore 
mother  cells,  and  after  this  division  a  smaller  number  of  chro¬ 
mosomes  than  before  is.  present,  there  can  be  little  doubt  that  in 
microspore  formation  reduction  takes  place,  and  that  the  x  and 
2%  generations  are  characterized  respectively  by  19  and  38  chro- 


1914] 


M  A  NE  V  A  L—M  A  GNOLIA  CEA  E 


3 


mosomes.  Neither  Strasburger  (29)  nor  Andrews  (i)  deter¬ 
mined  the  exact  number  of  chromosomes  in  the  forms  studied  by 
them. 

The  mature  pollen  grains  are  oval  in  shape,  with  rather  thick 
walls.  In  the  case  of  Magnolia  they  are  binucleate  (fig.  21),  while 
those  of  Liriodendron  are  two-celled  (fig.  4).  This  condition  is 
found  in  the  anthers  before  dehiscence  occurs,  which,  in  the  latter 
species,  is  between  May  15  and  18,  and  in  the  former  about  May  30. 

In  early  stages  of  development  it  is  evident  that  the  tapetum 
arises  from  the  sporogenous  tissue  (fig.  15),  later  differing  from  it 
especially  in  size  of  cells  and  nuclei  (fig.  17).  Still  later,  when 
tetrads  are  forming,  the  tapetum  consists  of  2  or  3  layers  of  large, 
binucleate  cells  lining  the  walls  of  the  loculi  (fig.  1).  Finally,  as 
the  pollen  grains  mature,  the  tapetum  gradually  disappears,  but 
there  is  no  evidence  of  migration  of  its  nuclei  among  the  develop¬ 
ing  pollen  grains  (fig.  18).  The  walls  of  the  loculi  consist  of  3  or  4 
layers  of  cells.  As  the  anthers  mature,  the  subepidermal  layer  of 
cells  becomes  differentiated  into  the  usual  type  of  cells  which  are 
active  in  dehiscence. 

The  ovules  in  both  Magnolia  and  Liriodendron  are  marginal  in 
origin  and  anatropous,  but  there  is  considerable  difference  in  the 
time  of  initiation  of  these  organs.  It  occurs  in  the  former  as  early 
as  the  first  two  weeks  in  December  or  earlier,  while  in  the  latter 
not  until  after  the  middle  of  March.  Early  in  April,  however,  the 
condition  attained  is  about  the  same  in  both,  and  the  two  develop 
at  the  same  rate  until  the  completion  of  the  embryo  sac.  The  first 
rudiment  of  the  inner  integument  appears  when  the  megaspore 
mother  cell  is  well  differentiated  (April  20),  and  soon  afterward 
the  outer  integument  is  initiated  (fig.  5).  From  the  archesporial 
cell  (fig.  22)  a  tapetal  cell  is  cut  off  (fig.  23),  apparently  in  both 
species,  and  the  mother  cell  soon  becomes  deeply  buried  within  the 
nucellus  (fig.  24).  By  two  successive  divisions  of  the  megaspore 
mother  cell  4  megaspores  are  formed  (figs.  6,  7,  25,  26,  27),  the 
innermost  of  these  in  each  case  being  functional,  while  the  others 
degenerate.  By  the  time  the  4  megaspores  have  developed  the 
innermost  one  comes  to  lie  very  deep  within  the  nucellus  (fig.  7). 

The  development  of  the  embryo  sac  is  normal  throughout. 


4 


BOTANICAL  GAZETTE 


[JANUARY 


Even  in  the  binucleate  condition  the  sac  is  considerably  elongated 
(fig.  28);  it  continues  to  grow  more  in  length  than  in  breadth; 
finally  it  becomes  slightly  curved  and  also  somewhat  enlarged  at 
the  ends.  The  tetranucleate  sac  is  shown  in  fig.  29.  The  mature 
sac  is  of  the  ordinary  type,  containing  an  egg  and  two  beaked  syner- 
gids  at  the  micropylar  end,  three  antipodals  at  the  opposite  end, 
and  two  endosperm  nuclei  somewhat  above  the  middle  (figs.  8, 

9.  IO>  3°)- 

While  fertilization  was  not  observed  in  either  species,  there 
can  be  little  doubt  of  its  occurrence  in  both.  The  evidence  for  this 
is  that  when  material  of  a  certain  age  is  examined  the  remains  of 
the  pollen  tube  are  invariably  found  in  the  micropyle  and  also 
within  the  embryo  sac  (fig.  31). 

In  all  the  sacs  of  Magnolia  in  which  the  polar  nuclei  were  found, 
partial  fusion  had  already  occurred  (fig.  30).  After  fusion  the 
endosperm  nucleus  moves  close  to  the  egg  apparatus,  and  then, 
before  division  of  the  (presumably  fertilized)  egg,  the  first  division 
of  the  fusion  nucleus  takes  place.  At  this  division  a  wall  is  formed 
transverse  to  the  long  axis  of  the  embryo  sac  (fig.  31),  hence  the 
endosperm  is  cellular  from  the  start,  differing  from  Drimys  (29)  in 
this  respect.  Both  of  the  resulting  cells  participate  in  the  forma¬ 
tion  of  the  endosperm,  that  part  of  the  sac  surrounding  the  egg 
becoming  filled  with  endosperm  much  more  rapidly  than  the 
antipodal  end.  In  early  stages  the  endosperm  is  quite  compact 
(fig.  32),  but  later  the  cells  seem  to  enlarge;  finally,  in  the  mature 
condition,  the  nucellar  tissue  disappears  completely  and  an  abun¬ 
dant  supply  of  compact  endosperm  fills  the  seed. 

In  the  development  of  the  embryo  of  Magnolia  the  first  division 
is  transverse,  the  second  longitudinal  to  the  long  axis  of  the  embryo 
sac  (fig.  33).  A  second  longitudinal  wall  separates  the  young 
embryo  into  octants  (fig.  34),  and  soon  thereafter  the  divisions 
apparently  become  quite  irregular  (fig.  35).  There  is  much 
difference  in  the  form  of  different  embryos  of  approximately  the 
same  age,  some  being  nearly  globular  (fig.  35)  and  others  con¬ 
siderably  elongated.  A  well  defined  suspensor  (fig.  36)  appears 
somewhat  late  and  may  persist  until  the  embryo  is  mature.  The 
cotyledons  are  initiated  after  the  embryo  has  enlarged  considerably. 


1914] 


M  A  NE  V  A  L—M  A  GNOLIA  CEA  E 


5 


They  appear  simultaneously  and  are  independent  from  the  start, 
there  being  no  evidence  of  a  pseudo-monocotyledonous  habit  such 
as  occurs  in  various  other  members  of  the  Ranales.  In  the  mature 
seed  the  embryo  is  typically  dicotyledonous,  with  a  short  radicle 
and  well  developed  hypocotyl  and  cotyledons  (fig.  37). 

The  seed  coats  of  Magnolia  have  been  described  by  different 
botanists,  probably  the  earliest  correct  description  being  that  given 
by  Asa  Gray  (10).  In  the  mature  seed  the  outer  integument  is 
differentiated  into  two  layers,  an  outer  fleshy  one  well  filled  with 
oil  receptacles,  and  an  inner  stony  layer  of  bony  hardness.  The 
inner  integument  forms  only  a  thin  layer  in  the  ripe  seed.  After 
dehiscence  of  the  carpels  the  seeds  remain  suspended  a  few  days 
by  means  of  an  elastic  thread  formed  from  the  spiral  thickening 
bands  of  the  xylem  elements  of  the  raphe.  Finally  the  threads 
may  be  broken  and  the  seeds  fall  to  the  ground;  or  sometimes  the 
entire  cones  with  most  of  the  seeds  still  attached  are  shed.  This 
shedding  of  the  cones  results  from  a  break  across  the  base  of  the 
peduncle,  but  without  the  formation  of  a  definite  absciss  layer. 

In  the  case  of  Liriodendron  the  development  of  the  endosperm 
and  embryo  were  not  investigated. 

Before  discussing  the  embryo  sac  and  certain  other  points 
mentioned  above,  several  features  of  gross  structure  and  anatomy 
deserve  attention.  Arber  and  Parkin  (2)  define  the  term  flower 
as  “a  special  form  of  a  type  of  strobilus  common  to  angiosperms 
and  certain  mesozoic  plants,”  and  propose  to  designate  it  as  an 
anthostrobilus.  The  anthostrobilus  differs  from  all  other  strobili 
in  that  it  is  typically  amphisporangiate,  with  the  megasporophylls 
above  the  micro sporophy  11s  on  an  elongated  axis,  and  below  the 
sporophylls  a  distinct  perianth  which  is  wholly  or  partially  pro¬ 
tective.  The  angiospermous  type  of  anthostrobihis  is  called  a 
euanthostrobilus,  and  is  believed  by  them  primitively  to  have 
possessed  among  others  the  following  characteristics:  a  large  or 
indefinite  number  of  parts  arranged  spirally;  ovules  ortho tropous, 
several  in  each  ovary,  with  two  integuments;  marginal  placenta- 
tion;  filaments  short,  bearing  long  anthers  with  the  connectives 
prolonged  beyond  them;  members  of  the  perianth  all  similar, 
or  more  or  less  differentiated;  entomophilous.  The  flowers  of 


6  BOTANICAL  GAZETTE  [january 

Magnolia  and  Liriodendron  differ  from  the  above  type  only  in  hav¬ 
ing  anatropous  ovules  and  two-seeded  carpels.  In  the  proantho- 
strobilus  or  Bennettitean  type  of  “ flower”  corresponding  parts 
occur  with  a  similar  arrangement.  Arber  and  Parkin  hold  that 
“its  parts  are  homologous  with  the  carpels,  stamens,  and  perianth 
of  a  typical  amphisporangiate  angiospermous  flower.”  It  differs 
from  this,  however,  “  especially  in  the  presence  of  a  seminal  pollen¬ 
collecting  mechanism,  and  in  the  form  of  the  microsporophylls,” 
which  are  decidedly  fernlike.  More  details  regarding  the  proantho- 
strobilus  cannot  be  included  here,  but  may  be  found  in  the  well 
known  work  of  Wieland  (32). 

The  seedling  structure  of  Liriodendron  has  been  described  by 
Miss  Thomas  (30).  She  finds  here  a  form  intermediate  between 
the  normal  tetrarch  and  diarch  types  of  transition  from  cotyledons 
and  hypocotyl  to  root  as  found  in  the  Ranales,  Rhoedales,  and 
various  other  dicotyledons.  The  writer  has  confirmed  Miss 
Thomas’  descriptions.  The  peculiarity  in  Liriodendron  is  that 
while  in  the  cotyledons  and  upper  part  of  the  hypocotyl  the  struc¬ 
ture  is  that  ordinarily  occurring  in  connection  with  the  tetrarch 
type  of  root  (figs.  13,  14),  lower  down  in  the  hypocotyl  certain 
elements  disappear  so  that  the  root  is  diarch  (fig.  12).  On  account 
of  lack  of  material  the  seedling  of  Magnolia  has  not  yet  been 
studied. 

In  both  gross  structure  and  anatomy  Magnolia  and  Liriodendron 
afford  many  points  of  similarity,  possessing  certain  characters 
common  to  all  Magnoliaceae  and  others  which  are  peculiar  to  the 
Magnolieae  (28, 2 1) .  Among  the  former  are  woody  stems,  alternate 
leaves,  secretory  cells,  a  characteristic  type  of  stoma,  and  more 
or  less  abundant  endosperm  in  the  seed;  the  latter  include  foliar 
stipules,  sclerenchymatous  diaphragms  in  the  pith,  and  the  bundles 
of  the  petiole  more  or  less  fused  in  an  irregular  ring. 

The  arrangement  of  the  vascular  bundles  in  the  peduncle  of 
Magnolia  and  in  the  petioles  of  Magnolia  and  Liriodendron  is 
shown  in  figs,  n,  38,  and  40,  and  details  of  the  petiolar  bundle  of 
Magnolia  are  represented  in  fig.  39.  Considering  the  Magnoliaceae 
as  a  whole,  the  petiolar  bundles  are  distributed  either  as  in  these 
two  species  or  in  the  form  of  a  crescent.  Parmentier  (21)  regards 


1914] 


M  A  NE  VA  L—M A  GNOLIA  CEA  E 


7 


the  different  arrangements  as  correlated  with  the  size  of  the  leaves. 
Worsdell  (33)  finds  medullary  bundles  in  the  petioles  of  various 
species  of  Magnolia ,  and  interprets  these  as  reminiscences  of  a 
primitive,  more  scattered  system  in  their  ancestors.  He  believes 
also  that  the  somewhat  irregular  system  of  bundles  in  the  peduncle 
of  Liriodendron  and  Magnolia  indicates  the  same  thing.  If  we 
accept  the  view  that  dicotyledons  have  been  derived  from  mono¬ 
cotyledons,  this  explanation  might  seem  more  or  less  plausible; 
however,  on  the  theory  that  monocotyledons  are  secondary,  this 
interpretation  could  hardly  be  correct. 

Present  theories  concerning  the  primitiveness  of  various  types 
of  angiospermous  embryo  sac  will  now  be  discussed.  According 
to  the  archegonium  theory  of  Porsch  (22),  the  8-nucleate  embryo 
sac  is  to  be  interpreted  as  the  equivalent  of  two  archegonia,  a 
micropylar  one  represented  by  the  egg  apparatus,  and  a  chalazal 
one  represented  by  the  three  antipodals.  Accepting  this  view, 
as  has  been  pointed  out  by  Brown  (3),  “we  might  conceive  of 
the  embryo  sac  of  Peperomia  as  really  composed  of  four  sacs,  each 
of  which  gives  rise  to  one  archegonium.”  A  similar  explanation 
might  hold  also  for  certain  other  anomalous  embryo  sacs  such  as 
are  found,  for  example,  in  the  Pennaeaceae.  Porsch,  however, 
in  his  paper  considers  only  the  8-nucleate  type. 

This  theory  has  been  criticized  from  various  standpoints.  In 
the  gymnosperms,  for  instance  (3),  in  all  species  that  form  arche¬ 
gonia,  the  megaspore  first  produces  a  non-cellular  stage  of  the 
gametophyte,  and  subsequently  a  cellular  stage  in  all  species  that 
form  archegonia ;  and  it  is  in  this  cellular  tissue  that  the  archegonia 
are  initiated  and  formed.  So  if  we  homologize  the  first  two  divisions 
of  the  ordinary  angiospermous  embryo  sac  with  the  free  nuclear 
divisions  of  the  gymnospermous  prothallus,  the  shifting  of  the 
archegonia  from  the  cellular  to  the  non-cellular  stage  of  the  pro¬ 
thallus  must  be  explained. 

Ernst  (9)  admits  that  the  archegonium  theory  would  be 
sehr  bestechend  if  within  the  8-nucleate  embryo  sac  the  two  groups 
of  nuclei  were  always  of  nearly  the  same  form.  The  numerous 
variations  from  the  “normal”  type,  not  only  in  the  form  of  the 
egg  apparatus  and  of  the  antipodal  apparatus,  but  also  in  the 


8 


BOTANICAL  GAZETTE 


[JANUARY 


behavior  of  the  polar  nuclei,  serve,  he  believes,  better  to  refute 
than  to  support  Porsch’s  theory. 

.  Other  valid  criticisms  might  be  offered,  but  we  need  not  do 
this  here,  since,  even  if  we  were  to  accept  the  theory,  the  question 
as  to  the  most  primitive  type  of  angiospermous  embryo  sac  would 
still  remain  unsolved. 

In  a  recent  publication  (9)  Ernst,  after  considering  the  course 
of  development  of  the  ordinary  angiospermous  embryo  sac,  as  well 
as  of  such  peculiar  types  as  occur  in  Gunnera  macrophylla ,  Peperomia 
pellucida,  P.  hispidula ,  and  the  Pennaeaceae,  arrives  at  conclu¬ 
sions  quite  different  from  those  published  slightly  earlier  by 
Coulter  (5).  According  to  Coulter,  the  most  important  of  the 
five  nuclear  divisions  in  the  development  of  the  ordinary  embryo 
sac  are  the  first  two,  which  result  in  the  formation  of  tetrads. 
Coulter  asserts  that,  so  far  as  we  know,  if  fertilization  is  to  occur 
later,  the  reduction  divisions  are  not  omitted;  and  that  whether 
the  number  of  divisions  of  the  embryo  sac  mother  cell  is  reduced 
from  5  to  4,  or  even  to  3,  the  reduction  divisions  are  never  omitted. 
In  such  forms  as  Peperomia ,  in  spite  of  the  fact  that  the  embryo 
sac  contains  16  nuclei,  there  are  only  4  divisions  of  the  embryo 
sac  mother  cell,  instead  of  5  as  in  the  ordinary  8-nucleate  type 
of  embryo  sac. 

To  this  view  Ernst  replies:  “Die  Entwicklungsvorgange  im 
Embryosack  scheinen  mir  unabhangig  von  seiner  Entstehung 
betrachtet  werden  zu  miissen.”  So  Ernst  holds  that  although 
the  omission  of  tetrad  formation  is  a  reduction  of  the  course  of 
development  and  not  a  primitive  character,  it  has,  nevertheless, 
no  influence  on  the  development  of  the  embryo  sac,  and  that  the 
5  divisions  of  the  embryo  sac  mother  cell  resulting  in  the  8-nucleate 
sac  belong  to  two  entirely  different  phases  of  development;  that 
is,  formation  of  spores,  characterized  by  reduction  of  chromosomes, 
and  germination  of  spores,  characterized  by  polarity,  number  of 
nuclear  divisions,  position  of  nuclei,  development  of  vacuoles,  and 
cell  formation. 

It  is  evident  that  Coulter  regards  the  16-nucleate  embryo 
sac  of  such  forms  as  Peperomia  as  derived  by  a  reduction  of  the 
divisions  of  the  embryo  sac  mother  cell  to  4  instead  of  5.  Ernst, 


1914] 


M  A  NE  V  A  L—MA  GNOLIA  CEA  E 


9 


on  the  other  hand,  sees  here  an  omission  of  tetrad  formation  and 
one  more  than  the  usual  number  of  divisions  in  the  germination  of 
the  megaspore  to  the  embryo  sac.  He  therefore  considers  the 
16-nucleate  sac  as  an  older,  or  at  any  rate  an  independent,  form 
of  embryo  sac,  not  derived  from  the  8-nucleate  type.  These  two 
views,  then,  are  directly  opposed  to  each  other. 

With  respect  to  the  nature  of  the  16-nucleate  embryo  sac  of 
Peperomia ,  Campbell  (4)  and  Johnson  (15,  16),  as  is  well  known, 
have  arrived  at  opposite  conclusions.  Campbell  says :  ‘ ‘  Peperomia , 
in  regard  to  the  embryo  sac,  probably  represents  the  most  primitive 

form  yet  discovered  among  the  angiosperms . Peperomia 

offers  a  basis  for  an  explanation  of  the  homologies  of  the  embryo 
sac.”  Johnson,  a  little  later,  after  studying  several  genera  of 
Piperaceae,  maintained  that  the  peculiarities  in  Peperomia  are  of 
secondary  origin.  The  latter  view  is  supported  by  Brown  (3) 
who,  in  Peperomia  sintenisii  and  P.  arifolia,  finds  that  at  the  first 
two  divisions  of  the  embryo  sac  mother  cell  typical  reduction  of 
chromosomes  occurs;  and  also  that  during  these  divisions  the 
nuclei  are  separated  by  evanescent  cell  walls.  So  he  concludes 
that  these  phenomena  seem  to  indicate  that  the  sac  is  a  compound 
structure  derived  from  the  nuclei  of  four  megaspores,  the  primary 
sac  nucleus  being  a  mother  cell  rather  than  a  megaspore. 

Reference  has  been  made  to  Coulter’s  view  that  while  the 
genesis  of  the  ordinary  angiospermous  embryo  sac  from  the  mega¬ 
spore  mother  cell  involves  5  divisions,  the  essential  part  of  the 
process  is  found  in  the  first  two  divisions  which,  so  far  as  we  know, 
are  necessary  if  fertilization  is  to  occur.  Brown  (3)  maintains 
that  we  cannot  make  chromosome  reduction  the  sole  criterion  of 
megaspore  formation,  and  adds  as  another  distinction  that  while 
a  division  giving  rise  to  megaspores  is  characterized  by  a  cell  wall 
or  a  cell  plate,  the  first  division  of  a  megaspore  is  not  accompanied 
by  a  cell  plate.  Quite  lately  Smith  (27)  has  pointed  out  that 
this  distinction  does  not  hold  in  the  case  of  Clintonia ,  where,  at 
the  first  division  of  the  megaspore  nucleus,  a  cell  plate  appears, 
and  Smith  infers  it  will  not  hold  for  certain  other  cases. 

Sufficient  emphasis,  it  seems  to  the  writer,  has  never  been  given 
to  the  fact  that  while  the  anomalous  types  of  embryo  sac  are  as  a 


IO 


BOTANICAL  GAZETTE 


[JANUARY 


rule  of  rare  occurrence  and  are  distributed  among  entirely  unrelated 
families,  on  the  other  hand,  the  ordinary  8-nucleate  type  developed 
by  5  divisions  of  the  megaspore  mother  cell  occurs  in  nearly  all 
families  of  angiosperms  from  the  most  primitive  to  the  most 
specialized.  This  is  significant  and  is  hardly  to  be  explained  on 
any  other  hypothesis  than  that  the  latter  type  is  primitive.  We 
have  in  the  8-nucleate  sac,  it  seems,  a  structure  of  marvelous 
constancy  in  development  and  arrangement  of  parts,  evolved  in 
the  course  of  long  ages,  the  exceptions  to  which  only  strengthen 
the  view  that  it  is  a  primitive  type  of  embryo  sac. 

Another  reason  for  regarding  anomalous  types  of  embryo  sac 
as  derived  is  the  variability  in  the  manner  of  their  development. 
This  is  especially  marked  in  the  case  of  16-nucleate  sacs,  where  a 
peculiar  method  of  development  is  found  in  almost  every  new  case 
discovered.  Of  course  it  may  be  objected  that  these  variations 
are  of  minor  importance.  But  even  if  this  were  true,  it  certainly 
contrasts  strikingly  with  the  remarkable  uniformity  so  very  general 
even  in  minor  details  of  the  development  of  the  ordinary  angio- 
spermous  type,  and  is  a  fact  to  be  explained. 

Whether  or  not  we  consider  the  first  4  nuclei  produced  by 
division  of  the  embryo  sac  mother  cell  as  megaspores,  and  this  view 
seems  reasonable  in  most  cases,  is  probably  of  less  importance  than 
many  have  believed.  The  genesis  of  the  angiospermous  sporo- 
phyte,  aside  from  the  exceptional  cases  such  as  those  involving 
apogamy  and  budding,  always  begins  with  a  perfectly  definite 
structure,  the  embryo  sac  mother  cell.  If  fertilization  is  to  occur 
later,  then,  without  exception,  reduction  of  chromosomes  takes 
place  at  the  first  two  divisions  of  this  cell.  Now,  considering 
parthenogenesis  as  a  secondary  phenomenon,  we  see  that  in  the 
development  of  all  normal  embryo  sacs  (that  is,  those  capable  of 
being  fertilized),  whatever  their  type  of  mature  structure,  there  is 
this  common  feature  in  development.  After  the  reduction  divisions 
the  embryo  sac  may  develop  as  the  product  of  one-fourth,  one-half, 
or  all  of  the  four  reduced  nuclei  derived  from  the  original  mother 
cell.  The  ordinary  8-nucleate  type  develops  as  the  product  of 
one-fourth  of  these  nuclei  by  three  successive  divisions;  the  sac 
of  Cypripedium  (20)  develops  as  the  product  of  one-half  of  these 


MANEVAL—MAGNOLIACEAE 


II 


1914] 


nuclei  by  one  division ;  that  of  Lilium  as  the  product  of  all  of  these 
nuclei  by  one  division;  and  that  of  Peperomia  from  all  of  these 
nuclei  by  two  divisions.  The  three  latter  cases  clearly  show  an 
abbreviation  in  the  course  of  development  of  the  gametophyte, 
whether  we  regard  that  course  as  beginning  with  the  embryo  sac 
mother  cell  or  after  chromosome  reduction. 

That  we  cannot  make  chromosome  behavior  the  sole  criterion 
for  distinguishing  sporophyte  and  gametophyte  is  doubtless  true. 
This  is  evident  from  chromosome  behavior  in  cases  of  partheno¬ 
genesis  such  as  occur  in  Alchemilla  (19),  and  in  the  numerous 
instances  of  apogamy  and  apospory  among  both  pteridophytes 
and  spermatophytes.  However,  it  is  probable  that  no  one  has 
ever  dreamed  of  making  such  unusual  phenomena  the  basis  of  any 
theory  of  the  nature  or  phylogeny  of  the  angiospermous  embryo 
sac.  These  phenomena  undoubtedly  are  secondary.  Hence  the 
conception  that  chromosome  behavior  is  the  most  important 
criterion,  at  least  in"  all  cases  where  fertilization  occurs,  seems  well 
founded.  So  if  abbreviation  in  the  developmental  history  of  the 
gametophyte  in  angiosperms  expresses  an  evolutionary  tendency 
which  can  be  traced  back  as  far  as  the  gametophyte  of  the  pterido¬ 
phytes,  then  anomalous  embryo  sacs  are  secondary  rather  than 
primitive  types. 

If  now  the  embryo  sacs  of  those  Magnoliaceae  thus  far  investi¬ 
gated  are  considered,  no  clue  is  discovered  in  their  development  or 
structure  as  to  the  primitiveness  of  the  group;  and  this  for  the 
simple  reason  that,  although  we  regard  this  type  as  the  most 
primitive  among  angiosperms,  yet  the  same  type  is  the  common 
one  among  all  angiosperms.  Moreover,  whatever  theory  we  accept, 
the  past  study  of  the  embryo  sac  has  served  mainly  to  emphasize 
the  vast  difference  between  angiosperms  and  lower  groups  of  plants 
in  this  respect,  and  so  to  increase  rather  than  to  bridge  the  wide 
gap  between  them.  It  would  seem  then  that  if  the  problem  of  the 
origin  of  angiosperms  is  to  be  solved  this  must  come  about  princi¬ 
pally  as  a  result  of  investigations  of  other  features  than  the  embryo 
sac. 

During  the  last  two  decades  the  amount  of  purely  descriptive 
literature  dealing  with  embryo  sacs  has  grown  to  huge  proportions, 


12 


BOTANICAL  GAZETTE 


[JANUARY 


but  the  different  theories  as  to  which  type  is  primitive  have  not 
been  reconciled.  If,  however,  anomalous  types  of  angiospermous 
embryo  sacs  are  secondary  and  not  primitive,  as  seems  most 
reasonable,  then  the  causes  of  these  secondary  modes  of  develop¬ 
ment  should  be  investigated.  This  is  obviously  a  problem  present¬ 
ing  serious  difficulties,  yet  they  are  probably  not  insurmountable. 
A  key  to  the  situation  may  probably  be  found  by  considering  the 
possibility  that  there  is  some  relation  between  anomalous  types 
of  embryo  sac  development  and  peculiar  environmental  conditions. 
This  has  been  suggested,  for  example,  by  Johnson  (15). 

Since  the  strobilus  theory  of  Arber  and  Parkin  (2)  is  based 
so  largely  on  a  comparison  of  the  flower  (euanthostrobilus)  of 
angiosperms  and  the  proanthostrobilus  of  the  Bennettitales,  we 
must  refer  to  certain  views  as  to  the  nature  of  these  structures. 
Arber  and  Parkin,  agreeing  with  Hallier  (ii)  and  Senn  (26), 
consider  the  amphisporangiate  flower  of  Magnolia  and  Liriodendron 
as  made  up  of  sporophylls  and  perianth  borne  directly  on  the  main 
axis  of  the  floral  shoot  rather  than  as  a  compound  structure.  This 
they  regard  as  the  most  primitive  type  of  angiospermous  flower, 
reproducing  the  essential  features  of  the  Bennettitean  strobilus. 
Wettstein  (31)  and  others,  on  the  contrary,  think  that  the  primi¬ 
tive  type  is  to  be  sought  for  among  the  monosporangiate  Apetalae, 
and  that  the  angiospermous  fructification  is  a  reduced  inflorescence, 
derived  from  that  of  the  gymnosperms.  Lignier  (17),  at  least, 
interprets  the  Bennettitean  strobilus  also  as  a  compound  structure, 
an  inflorescence.  It  is  clear  that  conclusions  as  to  the  primitive¬ 
ness  of  different  groups,  as  well  as  to  the  origin  of  angiosperms  as 
a  whole,  will  vary  according  to  which  of  these  views  is  accepted. 

The  greatest  differences  between  the  two  theories  have  been 
indicated.  Whether  the  primitive  angiospermous  flower  was 
anemophilous  or  entomophilous  is  perhaps  of  relatively  minor 
importance,  yet  this  question  also  is  involved  in  both  of  these 
theories.  It  would  seem  natural  to  imagine  anemophily  as  the 
method  of  pollination  among  primitive  angiosperms,  yet  if  ento- 
mophily  has  played  as  important  a  role  as  many  suppose  in  their 
evolution,  from  their  very  origin,  then  the  latter  must  be  primitive 
for  this  group. 


IQ1 4] 


M  A  NE  VA  L—MA  GNOLIA  CEA  E 


13 


Thus  far  the  monocotyledons  have  been  left  out  of  account 
in  looking  for  primitive  angiosperms.  Let  us  now  turn  to  this 
group. 

The  remarkable  uniformity  in  the  development  and  mature 
condition  of  the  male  and  female  gametophytes  of  monocotyledons 
and  dicotyledons  has  been  brought  forth  repeatedly  as  the  strongest 
argument  in  favor  of  a  monophyletic  theory.  In  spite  of  objections 
such  as  the  claim  that  “  similarity  in  structure  may  be  the  out¬ 
growth  of  the  changes  that  resulted  in  the  evolution  of  seeds” 
(6),  it  seems  that  we  are  far  from  the  point  of  even  thinking  of 
abandoning  this  as  well-nigh  irrefutable  evidence  of  close  genetic 
relationship  between  the  two  great  classes  of  angiosperms. 

Within  the  last  few  years  the  striking  similarity  in  the  seedling 
structure  of  dicotyledons  and  monocotyledons  has  been  demon¬ 
strated  in  many  forms.  Although  the  generalization  that  “  onto¬ 
geny  repeats  phylogeriy”  has  likely  been  overworked,  yet  if  there 
is  anything  at  all  in  this  rule,  then  the  evidence  from  seedling 
structure  deserves  its  full  share  of  consideration. 

In  favor  of  the  view  that  the  two  groups  have  originated  in¬ 
dependently  are  the  differences  in  their  anatomy,  and  in  the 
development  and  mature  condition  of  the  embryo.  As  a  result  of 
recent  study,  however,  we  learn  that  anatomically  the  structure 
of  seedlings  in  particular,  but  also  of  mature  individuals  in  the 
two  groups,  offers  many  striking  points- of  resemblance.  Other 
differences,  generally  regarded  as  secondary  in  importance,  are 
seen  in  the  venation  of  the  leaves,  in  the  grandifoliate  as  opposed 
to  the  parvifoliate  habit,  and  in  floral  symmetry. 

The  principal  resemblances  and  differences  between  monocotyle¬ 
dons  and  dicotyledons  on  which  present  phyletic  theories  are  based 
have  been  mentioned.  In  reviewing  these  theories  we  may  recall 
the  fact  that  while  according  to  most  if  not  all  monophyletic  theories 
proposed  until  recently,  dicotyledons  were  assumed  to  be  derived 
from  monocotyledons,  students  of  phylogeny  today  quite  generally 
hold  the  opposite  view.  Worsdell  (33),  however,  is  still  inclined 
to  the  view  that  monocotyledons  rather  than  dicotyledons  are 
primitive.  He  believes  that  “  angiosperms  have  developed  directly 
from  an  ancestor  belonging  to  the  bryophytic  level,  and  that  they 


14 


BOTANICAL  GAZETTE 


[JANUARY 


have  not  come  from  either  gymnosperms,  pteridosperms,  or  ferns.” 
His  conclusion  is  based  mainly  on  the  following  insufficiently 
substantiated  assumptions:  that  taking  the  vegetable  kingdom 
as  a  whole,  the  grandifoliate  habit  is  primitive,  the  parvifoliate 
derived;  that  the  appearance  of  two  cotyledons  in  dicotyledons 
is  illusive,  there  really  being  only  one  which  is  deeply  bifurcated; 
that  in  the  monocotyledonous  seedling  there  is  no  room  for  the 
scattered  arrangement  of  the  bundles,  so  we  cannot  on  account 
of  its  absence  here  conclude  that  the  scattered  condition  has  been 
derived  from  a  vascular  cylinder.  These  points  cannot  be  dis¬ 
cussed  here ;  it  suffices  to  say  that  the  criticism  that  this  view 
assumes  entirely  too  much  seems  fair.  Besides,  the  evidence  from 
fossils  is  entirely  against  it,  the  general  conclusion  of  paleobotanists 
being  that  from  the  Bryophyta  no  higher  forms  have  ever  evolved. 
Scott  (25),  touching  this  point,  says:  “ neither  among  living  nor 
fossil  plants  has  any  indication  of  a  structure  intermediate  between 
the  plant  of  a  vascular  cryptogam  and  the  fruit  (sporophyte)  of  a 
bryophyte  ever  been  discovered.” 

The  view  that  monocotyledons  have  been  derived  from  dicoty¬ 
ledons,  doubtless  at  a  rather  early  period  in  the  history  of  angio- 
sperms,  and  possibly  by  branching  from  several  points  along  the 
dicotyledonous  line,  has  been  much  strengthened  by  the  researches 
of  the  last  15  years.  Miss  Sargant  (24)  regards  the  common 
characters  of  monocotyledons  and  dicotyledons  as  too  numerous 
and  uniform  to  have  been  acquired  independently,  and  emphasizes 
the  fact  that  angiosperms  are  especially  unique  with  respect  to 
their  flowers,  carpels,  and  endosperm.  The  attainment  of  practical 
identity  in  the  “  germination  of  the  embryo  sac  and  the  history  of 
the  endosperm”  by  independent  evolution  among  monocotyledons 
and  dicotyledons  “would  require  a  series  of'  coincidences,”  she 
says,  “so  improbable  as  to  be  inconceivable.”  With  respect  to  the 
flower,  Miss  Sargant  agrees  with  the  view  of  Arber  and  Parkin 
given  elsewhere. 

Probably  Miss  Sargant’s  most  important  contribution  to  the 
monophyletic  theory  is  based  on  anatomical  investigations.  The 
presence  or  absence  of  a  cambium  seems  to  account  largely  for  the 
difference  in  detail  between  monocotyledonous  and  dicotyledonous 


1914] 


MANEVAL — MAGNOLIACEAE 


IS 


stems,  hence  the  great  importance  of  any  evidence  as  to  its  presence 
among  primitive  angiosperms.  That  a  true  cambium  develops 
in  certain  monocotyledons  ( Gloriosa ,  23)  is  now  well  known;  but 
especially  significant  is  the  fact  that  while  the  structure  of  the 
mature  stem  of  monocotyledons  and  dicotyledons  generally  varies 
greatly,  the  primary  structure  of  the  dicotyledonous  stem,  which 
is  the  same  in  seedlings  and  mature  plants,  is  also  frequent  in 
monocotyledonous  seedlings.  So  in  the  light  of  this  evidence  and 
also  of  the  fact  that  a  cambium  is  usually  present  among  living 
gymnosperms  and  extinct  vascular  cryptogams,  and  is  universally 
present,  so  far  as  known,  among  extinct  gymnosperms,  the  view 
that  primitive  angiosperms  possessed  a  cambium  seems  well 
founded. 

The  argument  for  most  of  Miss  Sargant’s  other  views  cannot 
be  included  here,  yet  one  other  conclusion  should  be  mentioned. 
Since  among  gymnosperms  monocotyledonous  forms  are  unknown, 
and  the  dicotyledonous  condition  prevails,  one  would  naturally 
presume  that  the  embryo  of  primitive  angiosperms  was  dicotyle¬ 
donous;  besides,  the  embryological  development  of  angiosperms 
points  in  the  same  direction.  So  the  general  conclusion  is  that 
monocotyledony  is  secondary,  being  the  result  of  a  fusion  of  two 
cotyledons. 

Arber  and  Parkin  in  discussing  the  origin  of  angiosperms 
hold  ‘That  monocotyledons  branched  off  from  the  main  angio- 
spermous  line,  that  is,  dicotyledons,  at  a  very  early  period.” 
Since  the  embryo  of  Bennettites  was  dicotyledonous,  they  regard 
the  Hemiangiospermae  as  dicotyledonous  also,  and  so  conclude 
that  the  monocotyledonous  type  is  the  less  primitive  one.  In 
their  opinion  Miss  Sargant’s  explanation  of  the  monocotyledonous 
embryo  is  the  best  yet  offered.  They  also  recognize  the  need  of 
accounting  for  the  origin  of  the  monocotyledonous  habit. 

For  a  number  of  years  the  so-called  anomalous  dicotyledons 
have  attracted  students  in  the  hope  that  knowledge  of  their 
embryos  and  anatomy  would  aid  in  solving  phylogenetic  problems. 
One  of  the  general  conclusions  of  such  investigations  is  that  the 
anomalous  characters  are  secondary  and  not  primitive  features. 
Mottier  (18),  for  example,  says,  “it  is  probably  true  without 


i6 


BOTANICAL  GAZETTE 


[JANUARY 


exception  that  dicotyledonous  plants  possessing  anomalous  embryos 
are  either  partially  or  wholly  geophilous  in  habit,  having  stems 
either  in  the  form  of  a  rhizome,  tuber,  or  a  short,  squat  axis.” 

That  anomalies  not  only  in  embryology  and  anatomy,  but 
even  in  embryo  sacs,  depend  largely  on  environmental  conditions 
has  been  suggested  in  the  past  (Johnson  15),  and  seems  continually 
to  be  receiving  wider  attention.  Hill  (14),  for  example,  has  dis¬ 
covered  in  the  Andes,  Central  America,  and  Mexico  a  few  geophilous 
species  of  Peperomia  which  are  of  great  interest.  Although  their 
seedlings  are  described  as  possessing  all  the  external  characters 
of  monocotyledons,  yet  they  are  true  dicotyledons,  but  the  coty¬ 
ledons  exhibit  a  marked  division  of  labor,  one  serving  for  absorp¬ 
tion,  the  other  for  photosynthesis.  That  these  species  are  true 
dicotyledons  is  shown  by  the  structure  of  the  seed;  the  presence 
of  stomata  on  the  lamina  of  the  absorbent  cotyledon;  persistence 
of  the  primary  root  for  some  time  after  the  formation  of  the  bulb; 
and  the  vascular  structure  of  the  seedling.  Moreover,  most  of 
the  members  of  the  genus,  containing  some  400  species,  are  nor¬ 
mally  dicotyledonous.  The  peculiar  habit  of  these  few  species 
is  therefore  interpreted  as  due  to  xerophytic  conditions,  resulting 
in  the  assumption  of  the  geophilous  habit,  accompanied  by  forma¬ 
tion  of  bulbs  or  tubers,  and  finally  affecting  even  the  embryonic 
structure  of  the  plants  so  that  the  division  of  labor  referred  to 
above  has  resulted.  Although  Hill  opposes  Miss  Sargant’s 
theory  as  to  the  origin  of  the  single  cotyledon  of  monocotyledons, 
it  is  worthy  of  note  that  he  attributes  the  anomalies  in  Peperomia 
to  the  geophilous  habit.  This  is  the  same  cause  that  other  workers 
have  assigned  for  the  pseudo-monocotyledonous  habit,  anomalous 
stem  structure,  and. so  on,  in  the  case  of  various  other  dicotyledons. 

Now  if  it  is  conceivable  that  a  pseudo-monocotyledonous  habit 
has  arisen  in  different  ways  among  dicotyledons,  then  the  possi¬ 
bility  of  the  same  thing  happening  among  monocotyledons  presents 
itself,  especially  if  monocotyledons  have  branched  off  at  several 
points  along  the  dicotyledonous  line.  Indeed,  attempts  at  a 
causal  explanation  of  the  origin  of  monocotyledons  from  dicoty¬ 
ledons  have  actually  been  made,  one  of  the  most  important  of 
these  being  Henslow’s  theory  (12). 


1914] 


MAN  EVA  L — M  A  GNOLIA  CEA  E 


17 


This  theory  is  founded  mainly  on  the  large  number  of  coin¬ 
cidences  among  both  dicotyledonous  and  monocotyledonous  aquatic 
plants,  and  on  the  fact  that  all  terrestrial  monocotyledons  exhibit 
the  same  coincidences.  Henslow,  as  well  as  many  others,  regards 
the  monocotyledons  as  degenerate  (when  compared  with  dicotyle¬ 
dons),  although  there  is  not  always  agreement  as  to  the  cause  of 
degeneracy.  Henslow  himself  believes  an  aquatic  habit  has  been 
the  principal  cause,  and  points  to  a  number  of  characteristics  of 
monocotyledons  and  dicotyledons  that  he  considers  the  result  of 
adaptation  to  a  moist  or  aquatic  environment.  Among  these 
peculiarities  are  large  size  of  leaves,  water  storage  organs,  the 
pseudo-monocotyledonous  condition  of  certain  dicotyledons,  early 
loss  of  primary  root,  and  “ endogenous”  arrangement  of  cauline 
bundles.  Henslow  remarks:  “In  the  title  of  my  first  paper  in 
1892  (13),  I  used  the  word  Theory,’  but  ....  I  feel  justified  in 
abandoning  the  term;  for  I  would  maintain  that  the  conclusion 
has  passed  the  stage  of  hypothesis  and  probability  only,  to  that 
of  a  demonstrated  fact”  While  it  is  likely  that  very  few  of  us 
would  be  willing  to  subscribe  to  this  conclusion,  yet  all  must 
agree  that  such  considerations  are  extremely  suggestive,  and 
indicate  a  line  of  work  that  is  promising,  especially  if  taken  up 
experimentally. 

To  multiply  examples  would  probably  not  add  to  the  force  of 
the  argument.  We  see  that  various  competent  workers  attribute 
anomalies  among  dicotyledons  to  a  geophilous  habit,  response 
either  to  xerophytic  or  to  hydrophytic  conditions.  Such  responses 
result  in  structural  peculiarities  in  stems,  formation  of  various 
types  of  underground  stems,  a  pseudo-monocotyledonous  habit, 
or  division  of  labor  among  the  cotyledons.  When  we  turn  to  the 
monocotyledons,  we  find  these  peculiarities  duplicated,  but  as  a 
rule  they  are  intensified.  That  their  production  is  related  to 
environment  seems  clearer  in  the  case  of  dicotyledons  than  of 
monocotyledons,  no  doubt  because  many  monocotyledons  at 
present  live  where  the  prevailing  conditions  do  not  seem  to  neces¬ 
sitate  geophily.  The  persistence  of  these  peculiarities  in  such 
environments  may  be  interpreted  as  retention  of  past  characters. 

It  seems  then  that,  on  account  of  many  similarities  between 


i8 


BOTANICAL  GAZETTE 


[JANUARY 


monocotyledons  and  anomalous  dicotyledons,  Henslow’s  conclu¬ 
sion  that  the  former  have  been  derived  from  the  latter  as  a  re¬ 
sponse  to  the  same  factors  that  determined  the  geophilous  habit 
is  reasonable,  at  least,  as  a  working  hypothesis.  Failure  to  recog¬ 
nize  the  fact,  however,  that  geophily  may  express  itself  variously 
has  sometimes  led  to  disagreement  in  theories  where  none  actually 
exists.  This  appears  especially  in  discussions  of  the  origin  of  the 
monocotyledonous  from  the  dicotyledonous  habit,  it  being  held 
that  monocotyledony  has  arisen  in  only  one  way.  There  are  at 
least  three  plausible  theories  concerning  the  method  by  which  this 
may  have  occurred:  first,  by  suppression  of  one  of  two  cotyfedons; 
next,  by  fusion  of  two  cotyledons;  and,  finally,  by  a  division  of 
labor  between  two  cotyledons.  Now  since  we  find  a  difference  in 
the  behavior  of  the  cotyledons  in  certain  anomalous  dicotyledons, 
it  is  entirely  probable  that  the  same  thing  has  happened  in  the 
origin  of  monocotyledons  from  dicotyledons,  so  much  the  more 
so  if  there  is  more  than  one  monocotyledonous  branch  from  the 
primitive  dicotyledonous  stock. 

While,  as  has  been  shown,  the  most  generally  accepted  view  is 
that  angiosperms  are  monophyletic  we  must  also  remember  the 
possibility  of  a  diphyletic  origin.  Coulter  (6)  has  expressed  his 
view  on  this  point  as  follows:  “In  our  judgment  the  evidence  is 
strongly  in  favor  of  the  independent  origin  of  the  two  groups, 
which  have  attained  practically  the  same  advancement  in  the 
essential  morphological  structures,  but  are  very  diverse  in  their 
more  superficial  features.  Their  great  distinctness  now  indicates 
either  that  they  were  always  distinct  or  that  they  originated  from 
forms  that  were  really  proangiosperms  and  neither  monocotyledons 
nor  dicotyledons.”  Those  who  hold  this  view  will  have  to  explain 
more  satisfactorily  than  has  been  done  the  similarity  between 
monocotyledons  and  dicotyledons  in  gametophytic  development 
and  in  seedling  structure;  the  general  similarity  between  mono¬ 
cotyledons  and  anomalous  dicotyledons;  and  the  evidence  that 
primitive  angiosperms  possessed  a  cambium  and  were  dicotyle¬ 
donous.  The  monophyletic  theory  has  been  strongly  reinforced 
in  recent  years  and  the  writer  finds  it  more  acceptable  than  the 
diphyletic,  but  more  evidence  is  needed  before  it  can  be  unreservedly 
accepted. 


1914] 


MAN  EVA  L—MA  GNOLIA  CEA  E 


19 


It  is  evident  then,  from  the  above  considerations,  .that  we 
regard  the  Magnoliaceae,  since  they  belong  to  the  more  primitive 
group  of  angiosperms,  as  more  primitive  than  the  monocotyledons. 
Let  us  next  consider  certain  theories  relative  to  the  primitiveness 
of  various  features  among  the  dicotyledons  themselves. 

Present  theories  on  this  subject  are  fairly  well  represented  by 
the  views  of  Wettstein  (31)  on  the  one  hand  and  those  of  Arber 
and  Parkin  (2)  on  the  other.  Both  believe  that  monocotyledons 
have  been  derived  from  dicotyledons.  Wettstein  holds,  because 
of  similarity  in  cotyledons,  stem,  floral  structure,  and  reduction  of 
the  primary  root,  that  monocotyledons  have  been  derived  from  the 
Polycarpicae.  He  also  points  out  that  while  we  may  think  of 
derivation  of  one  cotyledon  from  two,  the  reduction  of  a  primary 
root,  and  so  on,  the  opposite  would  not  seem  possible  under  any 
circumstances.  So  he  concludes  that  we  must  turn  to  the  dicoty¬ 
ledons  in  considering  the  phylogeny  of  angiosperms,  but  disagrees 
entirely  with  many  as  to  which  dicotyledons  are  most  primitive. 

Both  theories  derive  angiosperms  from  gymnosperms.  Accord¬ 
ing  to  Wettstein,  primitive  angiosperms  should  present  among 
others  the  following  characteristics:  prevalence  of  woody  plants 
and  absence  of  vessels  in  the  vascular  bundles;  prevalence  of 
monosporangiate  flowers,  with  either  no  perianth  or  one  of  simple 
structure;  prevalence  of  anemophily.  These  are  gymnospermous 
characters,  and  Wettstein  holds  that  we  should  regard  that  group 
of  angiosperms  as  most  primitive  which  exhibits  these  characters 
developed  in  high  degree.  Arber  and  Parkin  (2),  Hallier  (ii), 
and  others  give  a  much  longer  list  of  characters  which  they  believe 
are  primitive.  According  to  their  views,  amphisporangiate,  actino- 
morphic  flowers,  with  elongated  axes  bearing  numerous  free,  spirally 
arranged  floral  parts,  are  primitive.  Such  flowers  also  possess  a 
well  developed,  undifferentiated  perianth  and  are  entomophilous. 
Besides,  primitive  angiosperms  are  dicotyledonous,  have  small  em¬ 
bryos  and  abundant  endosperm,  are  treelike,  and  lack  true  vessels 
among  autophytic  species. 

If  it  is  granted  that  all  the  essential  characters  that  may  be 
regarded  as  primitive  have  been  included  in  these  lists,  then  it  is 
evident  that  the  great  differences  between  the  two  theories  relate 


20 


BOTANICAL  GAZETTE 


[JANUARY 


to  but  a  few  points,  points  which  involve,  however,  no  end  of 
difficulty.  The  two  theories  would  apparently  be  reduced  to  one 
if  we  could  say  which  of  the  following  are  primitive:  monospo- 
rangiate  or  amphisporangiate  flowers;  presence  or  absence  of  a 
perianth;  anemophily  or  entomophily.  Of  possibly  less  impor¬ 
tance  is  the  question  whether  the  angiospermous  flower  is  a  modified 
simple  (that  is,  unbranched)  shoot  or  a  modified  infloresence.  There 
is  agreement  as  to  the  primitiveness  of  such  characters  as  actino- 
morphy,  freedom  of  floral  parts,  dicotyledony,  lack  of  true  vessels 
in  the  vascular  strands,  and  prevalence  of  woody  plants.  So  it 
seems  important  to  discuss  the  differences  cited. 

The  fact  that  certain  characters  are  common  to  all  or  nearly  all 
gymnosperms  seems  in  many  instances  to  be  one  of  the  strongest 
reasons  for  regarding  those  characters  as  primitive  if  they  occur 
at  all  among  angiosperms.  Among  these  supposedly  primitive 
characters  are  dicotyledony,  prevalence  of  woody  plants,  and 
absence  of  tracheae  in  the  conducting  strands.  For  the  same  reason 
we  might  conclude  that  primitive  angiosperms  were  anemophilous 
and  possessed  naked,  monosporangiate  flowers,  since  these  char¬ 
acters  also  are  common  to  most  gymnosperms. 

Before  discussing  this  matter  further,  reference  may  be  made 
to  the  possibility  of  there  being  two  entirely  separate  lines  of  dicoty¬ 
ledons.  Reasons  have  been  given  for  believing  that  angiosperms 
are  monophyletic.  Now  if  the  similarity  between  dicotyledons 
and  monocotyledons  is  close  enough  to  warrant  such  a  conclusion, 
then,  since  the  similarity  is  so  much  more  striking  among  dicoty¬ 
ledons  themselves,  this  conclusion  seems  all  the  more  certain  in 
the  latter  case.  In  the  group  Dicotyledoneae  the  diversity  in  the 
development  and  structure  of  the  gametophytes  and  embryos  is 
surely  less  marked  than  is  the  diversity  among  angiosperms  as  a 
whole,  and  so  difficulties  are  increased  accordingly  if  any  other 
than  a  monophyletic  theory  is  proposed  for  the  phylogeny  of 
dicotyledons.  It  is  certainly  true  that  the  reproductive  structures 
and  organs  of  spermatophytes  are  among  their  least  plastic  features. 
While  it  is  dangerous  to  emphasize  too  strongly  the  importance  of 
even  the  most  stable  character  to  the  exclusion  of  others,  never¬ 
theless,  if  the  view  that  the  embryo  sac  points  unmistakably  to  a 


1914] 


M  A  NE  V  A  L — MA  GNOLIA  CEA  E 


21 


monophyletic  origin  of  angiosperms  is  incorrect,  a  more  satisfactory 
one  has  never  been  advanced.  The  homoplastic  explanation  seems 
well-nigh  inconceivable.  Besides,  in  the  morphological  and  ana¬ 
tomical  structure  of  seedlings  and  mature  plants  all  dicotyledons 
are  essentially  alike,  so  most  of  the  important  differences,  as  has 
been  indicated  above,  are  in  the  flowers.  Taking. all  the  evidence 
into  account  then,  it  seems  likely  that  all  dicotyledons  are  of  one 
stock,  and  that  the  monocotyledons  have  arisen  as  one  or  more 
branches  of  this  stock. 

If  then  dicotyledons  are  monophyletic,  which  are  the  most 
primitive?  If,  as  Arber  and  Parkin  (2),  Wettstein  (31),  and 
others  suppose,  they  have  been  derived  from  gymnosperms,  from 
what  particular  gymnospermous  stock  may  they  have  come  ? 
The  Gne tales  and  more  recently  the  extinct  Bennettitales  have 
each  been  thus  designated.  Even  if  dicotyledons  originated  from 
a  gymnospermous  stock,  opinions  will  differ  as  to  which  is  the 
parent  group,  depending  on  whether  one  regards  naked,  mono- 
sporangiate,  anemophilous  flowers,  or  entomophilous,  amphispo- 
rangiate  ones  with  a  perianth  as  primitive. 

The  entomophilous  habit  seems  clearly  associated  with  much 
in  the  evolution  of  angiosperms,  but  it  does  not  necessarily  follow 
that  primitive  angiosperms  were  entomophilous.  That  anemophi¬ 
lous  angiosperms  may  succeed  and  persist  in  competition  with 
entomophilous  forms  is  well  illustrated  by  such  groups  as  the 
Amentiferae  and  Gramineae. 

Few,  if  any,  believe  that  the  flower  of  any  existing  angiosperm 
is  like  the  primitive  angiospermous  flower.  Whether  this  primitive 
flower  was  monosporangiate  or  amphisporangiate  it  does  not 
follow,  though  this  is  quite  possible,  that  any  particular  flower 
of  today  is  the  direct  descendant  of  a  similar  type  in  its  ancestor. 
It  is  certain  that  in  many  instances  amphisporangiate  flowers  have 
become  monosporangiate,  and  that  perianths  have  been  more  or 
less  completely  lost. 

That  the  opposite  may  have  occurred,  however,  is  less  easily 
proven.  Arber  and  Parkin  (2),  for  example,  object  to  Engler’s 
view  (8)  that  the  monosporangiate  Apetalae  are  primitive  among 
dicotyledons,  by  saying  that  “it  must  be  assumed  that  the  perianth 


22 


BOTANICAL  GAZETTE 


[JANUARY 


is  evolved  de  now  and  is  an  organ  sui  generis But  suppose  we 
do  assume  that  primitive  angiosperms  possessed  a  perianth,  the 
origin  of  the  perianth  still  remains  to  be  explained.  Even  if  we 
say  that  it  is  a  direct  derivative  from  a  Bennettitean  ancestor, 
its  phylogenetic  origin  still  remains  a  mystery.  So  if  a  perianth 
developed  in  some  manner  or  other  among  the  Bennettitales, 
might  not  the  same  thing  have  occurred  among  angiosperms,  even 
long  after  they  became  a  distinct  group  of  plants  ? 

The  question  whether  primitive  angiospermous  flowers  were 
monosporangiate  or  amphisporangiate  presents  even  greater 
difficulties  than  that  concerning  the  primitiveness  of  the  perianth. 
If  angiosperms  have  descended  from  gymnosperms  we  would 
rather  expect  primitive  flowers  to  be  monosporangiate.  Evidence 
from  gymnosperms  that  amphisporangiate  flowers  are  primitive 
rests  almost  entirely  on  a  single,  extinct,  much  specialized  group 
of  plants,  the  Bennettitales.  This  group  no  doubt  represents,  as 
Coulter  (7)  suggests,  “the  end  of  a  gymnosperm  phylum.”  More¬ 
over,  that  the  proanthostrobilus  of  the  Bennettitales  corresponds 
closely  to  such  a  flower  as  that  of  Magnolia  or  Liriodendron  still 
remains  undecided.  The  resemblance  is  remarkable,  yet  if  the 
view  (17)  that  the  Bennettitean  inflorescence  is  a  compound  struc¬ 
ture  is  correct,  and  if  the  flower  of  Magnolia  is  not  compound,  then 
the  resemblance  becomes  only  a  superficial  one. 

If  then  we  go  back  far  enough  in  the  evolution  of  angiosperms, 
the  probability  seems  strong  that  the  group  was  monosporangiate. 
Amphisporangiate  flowers  are  unknown  below  angiosperms  except 
in  the  Bennettitales  and  possibly  Welwitschia.  Although  in  a 
number  of  respects  angiosperms  and  Gnetales  have  developed 
along  parallel  lines,  it  is  now  generally  believed  that  the  Gnetales 
are  not  transition  forms  leading  to  angiosperms.  This  view, 
however,  does  not  preclude  the  possibility  of  common  ancestry  in 
the  distant  past.  The  Gnetales  likely  represent  the  end  of  a 
gymnospermous  phylum  just  as  the  Bennettitales  do.  So  neither 
group  represents  the  direct  progenitors  of  angiosperms. 

Coulter  and  Chamberlain  (7)  say:  “It  is  recognized  that 
in  the  evolution  of  strobili  among  gymnosperms  there  were  prob¬ 
ably  two  distinct  tendencies:  a  monosporangiate  strobilus  (Cyca- 


1914] 


M  A  NE  VA  L—M  A  GNOLIA  CEA  E 


23 


dales,  Cordai tales,  Ginkgoales,  Coniferales),  and  a  bisporangiate 
strobilus  with  the  anthostrobilus  arrangement  of  sporophylls 
(Bennettitales,  Gnetales,  and  leading  to  angiosperms).”  This 
view  apparently  involves  the  idea  that  the  Bennettitales,  Gnetales, 
and  angiosperms  belong  to  one  stock,  but  the  relationship  between 
the  three  groups  at  their  origin  may  have  been  anything  but  close. 
Even  though  angiosperms  are  prevailingly  amphisporangiate  today 
this  may  not  have  been  the  condition  among  their  remote  ancestors; 
in  fact  it  seems  probable  that  those  ancestors  possessed  monospo¬ 
rangia  te  flowers. 

Though  primitive  angiosperms  possessed  monosporangia  te, 
naked,  anemophilous  flowers,  it  is  evident  that  they  did  not  become 
the  dominant  group  of  plants  until  they  developed  amphispo¬ 
rangiate  flowers  with  a  perianth,  and  became  entomophilous. 
This  view  is  evidently  opposed  to  the  one  that  the  present  day 
angiosperms  have  been  derived  from  the  Bennettitean  stock. 
The  main  reason  for  this  belief  is  that  except  for  resemblance  in 
the  fructifications,  which  may  be  quite  superficial,  the  two  groups 
are  entirely  different  in  structure.  Indeed,  had  the  Bennettitean 
proanthostrobilus  never  been  discovered,  probably  no  one  would 
have  ever  suspected  close  relationship  between  such  widely  differ¬ 
ent  groups.  Leaving  out  of  consideration  the  nature  of  the 
inflorescence,  the  following  may  be  noted  with  reference  to  the 
Bennettitales:  their  seeds  are  of  the  gymnospermous  type;  the 
microsporophylls,  microsporangia,  and  ramentum  are  fernlike  in 
character;  the  external  appearance  and  anatomy  of  the  stem  and 
leaf  indicate  relationship  with  cycads.  All  these  characters  suggest 
relationship  with  Cycadofilicales,  while  their  strobili  alone  indicate 
a  possible  connection  with  angiosperms.  It  seems  on  the  whole 
much  simpler  and  safer  to  conclude  that  the  Bennettitean  pro¬ 
anthostrobilus  and  the  angiospermous  anthostrobilus  are  nothing 
more  nor  less  than  the  results  of  homoplastic  development,  and 
that  if  they  indicate  relationship  at  all,  it  must  be  of  the  remotest 
kind,  dating  from  a  time  prior  to  the  origin  of  the  Bennettitales 
as  a  separate  stock,  a  time  when  neither  true  Bennettitales  nor 
angiosperms  had  ever  existed. 

If  then  angiosperms  were  primitively  anemophilous  with  naked 


24 


BOTANICAL  GAZETTE 


[JANUARY 


monosporangiate  flowers,  why  are  the  present  Monochlamydeae 
not  to  be  regarded  as  the  most  primitive  living  members?  This 
is  because  various  features  of  the  Monochlamydeae  indicate 
reduction  and  not  primitiveness.  If,  for  example,  the  entire 
group  as  constituted  by  Wettstein  (31)  be  considered,  it  is  found 
to  be  prevailingly  syncarpous.  This  surely  is  not  a  primitive 
feature.  Again,  in  various  families  there  are  closely  related  genera, 
even  species,  some  of  which  possess  a  perianth,  while  in  others  it 
is  rudimentary  or  entirely  absent.  It  is  difficult,  in  such  cases 
at  least,  to  conceive  of  the  latter  condition  as  primitive.  Besides, 
the  stamens  and  carpels  may  vary  in  number  even  in  closely 
related  genera  and  species.  That  the  smaller  numbers  in  such 
cases  are  derived  seems  to  be  a  reasonable  conclusion.  Moreover, 
the  inflorescences  among  the  Amentiferae,  for  example,  are  com¬ 
pound  structures  exhibiting  considerable  complexity.  This  too 
can  be  more  readily  interpreted  as  derived  and  not  primitive. 
Amphisporangiate  flowers  also  occur  in  certain  members  of  at 
least  7  families  included  by  Wettstein  among  the  Monochlamy¬ 
deae.  Such  cases  add  much  weight  to  the  view  that  the  mono¬ 
sporangiate  condition  throughout  the  group  is  secondary  and  not 
primitive. 

We  may  conclude  then  that  considering  existing  angiosperms, 
the  evidence  at  present  available  is  in  the  main  opposed  to  the 
view  that  they  have  been  derived  from  forms  at  all  closely  related 
to  the  Bennettitales.  The  one  striking  similarity  between  modern 
angiosperms  and  the  Bennettitales  may  well  be  a  result  of  homop- 
lasy.  Among  existing  angiosperms,  assuming  that  they  are 
monophyletic,  the  derivation  of  forms  having  monosporangiate, 
naked  flowers  from  those  possessing  amphisporangiate  flowers, 
bearing  an  undifferentiated  perianth,  seems  far  simpler  than  the 
reverse.  So,  .while  agreeing  with  Arber  and  Parkin,  Hallier, 
and  Senn  in  general  with  reference  to  those  features  which  they 
believe  are  primitive  among  existing  angiosperms,  there  seem  to 
be  no  very  adequate  grounds  for  concluding  that  primitive  angio¬ 
sperms  were  provided  with  entomophilous,  amphisporangiate 
flowers  bearing  a  perianth.  The  opposite  seems  much  more 
probable.  If  the  latter  is  true,  scarcely  a  suggestion  of  relation- 


1914] 


M  A  NE  V A  L—M  A  GNOLIA  CEA  E 


25 


ship  with  the  Bennettitales  remains.  But  even  if  the  former  is 
true,  it  would  seem  hazardous  to  hold  that  angiosperms  are  more 
closely  related  to  the  Bennettitean  stock  than  to  any  other  gymno- 
spermous  stock.  Coulter  and  Chamberlain  (7)  say  that  “the 
Cycadofilicales  are  so  fernlike  in  every  feature  except  their  seeds, 
that  their  derivation  from  some  ancient  fern  stock  (called  pro¬ 
visionally  Primofilices)  is  as  certain  as  phylogenetic  connections 
can  be.  The  origin  of  the  Cordaitales  therefore  presents  two 
alternatives:  either  they  arose  independently  from  the  same 
ancient  fern  stock,  or  they  were  differentiated  from  the  Cycado¬ 
filicales  very  early.”  The  same  two  alternatives  present  them¬ 
selves,  it  seems,  in  the  case  of  angiosperms.  Which  view  we  accept 
is  of  little  consequence  since  probably  neither  can  be  proven. 
Either  view  would  make  the  connection  between  angiosperms  and 
the  Bennettitales,  as  we  know  them,  a  most  distant  one. 

Let  us  now  turn  to  our  original  question  concerning  the  primi¬ 
tiveness  of  the  Magnoliaceae  among  existing  angiosperms.  While 
the  following  list  of  characters  of  the  Magnoliaceae  is  incomplete, 
it  doubtless  includes  most  of  the  more  important  ones  that  may 
be  considered  primitive:  (1)  the  ordinary  8-nucleate  type  of 
embryo  sac;  (2)  dicotyledony;  (3)  undifferentiated  perianth; 

(4)  amphisporangiate  flower;  (5)  entomophily;  (6)  elongated 

* 

conical  floral  axis;  (7)  actinomorphy;  (8)  indefinite  number  of 
free  floral  organs  arranged  spirally;  (9)  hypogyny;  (10)  apocarpy; 
(n)  woody  stems;  (12)  occasional  absence  of  tracheae  in  the 
vascular  bundles. 

It  is  quite  generally  agreed  that  the  last  7  of  these  characters 
are  relatively  primitive  wherever  found  among  angiosperms,  or 
if  not  that  they  are  of  minor  importance  as  evidence  of  phylogeny. 
The  first  two  characters,  since  they  are  common  to  nearly  all 
dicotyledons,  are  valueless  as  criteria  for  determining  primitiveness. 
There  are  left  three  characters  which  may  be  either  primitive  or 
derived,  namely,  undifferentiated  perianth,  amphisporangiate 
flowers,  entomophily.  These  three  characters  have  no  doubt 
developed  together  and  are  closely  bound  up  with  the  evolution 
of  angiosperms.  If  not,  then  naked,  monosporangiate,  anemophi- 
lous  flowers  must  indicate  primitiveness  where  found  in  existing 


26 


BOTANICAL  GAZETTE 


[JANUARY 


forms.  We  believe,  for  reasons  previously  given,  that  the  type  of 
flower  found  among  the  Magnoliaceae  is  primitive. 

The  present  investigation  adds  little  toward  the  solution  of 
the  plexus  of  problems  involved  in  the  origin  of  angiosperms  and 
the  relative  primitiveness  of  existing  groups.  An  opportunity  was 
offered,  however,  to  determine  whether  such  a  study  as  the  present 
one  of  a  possibly  primitive  group  of  angiosperms  might  yield  any 
results  of  either  positive  or  negative  value  as  a  contribution  to 
present  theories;  to  suggest  new  points  of  view  and  especially  to 
emphasize  certain  old  ones;  to  review  briefly  some  of  the  principal 
theories  of  the  present  day  on  the  primitiveness  and  origin  of 
monocotyledons  and  dicotyledons;  and  finally  to  criticize  where 
it  seemed  this  might  be  helpful  in  bringing  about  in  the  future 
reinforcement  or  correction  either  of  earlier  theories  or  of  the  view.^ 
expressed  in  this  paper. 

Summary 

1.  In  both  Magnolia  and  Liriodendron  the  sporogenous  tissue 
in  the  anther  is  differentiated  early  in  the  winter.  Tetrads  develop 
by  the  simultaneous  method  and  the  pollen  grains  when  mature  are 
binucleate  in  Magnolia ,  two-celled  in  Liriodendron.  The  tapetum 
originates  from  the  sporogenous  tissue. 

2.  The  x  number  of  chromosomes  in  each  species  is  19. 

3.  The  ovules  in  both  species  are  marginal,  anatropous,  and 
provided  with  two  integuments.  The  megaspore  mother  cell  in 
each  species,  by  two  successive  divisions,  produces  4  megaspores, 
of  which  the  innermost  is  functional.  The  mature  embryo  sacs 
are  of  the  ordinary  8-nucleate  type  and  fertilization  probably 
occurs  as  usual. 

4.  The  endosperm  of  Magnolia  is  cellular  from  the  beginning 
of  its  formation  and  is  abundant  in  the  mature  seed,  surrounding 
a  small,  typically  dicotyledonous  embryo.  The  first  division  in 
the  development  of  the  embryo  is  transverse,  the  second  longi¬ 
tudinal  to  the  long  axis  of  the  embryo  sac.  The  embryo  has  a 
well  defined  suspensor  and  no  evidence  of  monocotyledony  was 
found. 

5.  The  seed  of  Magnolia  possesses  three  coats:  an  outer  fleshy 


igi4\ 


M  A  NE  V  A  L—MA  GNOLIA  CEA  E 


27 


and  within  this  a  stony  one,  both  developed  from  the  outer  integu¬ 
ment,  and  a  thin  inner  one  from  the  inner  integument. 

6.  The  flowers  of  both  species  differ  from  the  euanthostrobilus 
of  Arber  and  Parkin  only  in  having  anatropous  ovules  and  two- 
seeded  carpels. 

7.  In  Liriodendron  the  seedling  possesses  in  the  cotyledons 
and  upper  part  of  the  hypocotyl  the  structure  generally  found 
associated  with  tetrarch  roots,  but  the  root  is  diarch. 

8.  All  Magnoliaceae  possess  certain  common  anatomical  char¬ 
acters,  while  others  are  peculiar  to  particular  groups.  The 
bundles  in  the  petioles  and  peduncles  of  Liriodendron  and  various 
species  of  Magnolia  are  somewhat  scattered,  a  feature  the  inter¬ 
pretations  of  which  vary. 

9.  Porsch’s  archegonium  theory  gives  no  suggestion  as  to 
what  type  of  angiospermous  embryo  sac  is  primitive. 

10.  A  consideration  of  all  available  evidence  in  the  light  of 
present  theories  very  strongly  favors  the  conclusion  that  the 
ordinary  8-nucleate  type  of  angiospermous  embryo  sac  is  the  most 
primitive.  But  in  view  of  its  wide  distribution  among  all  groups 
of  angiosperms,  its  occurrence  either  among  the  Magnoliaceae  or 
in  any  other  family  is  no  evidence  of  the  primitiveness  of  that 
family. 

11.  Angiosperms  are  believed  to  be  monophyletic,  especially 
on  account  of  the  uniformity  in  the  development  and  mature  con¬ 
dition  of  the  gametophytes,  and  because  of  similarity  in  seedling 
structure  of  monocotyledons  and  dicotyledons. 

12.  The  view  that  dicotyledons  have  been  derived  from  mono¬ 
cotyledons,  as  advanced  by  Worsdell,  rests  too  largely  on  assump¬ 
tion. 

13.  The  theory  that  monocotyledons  originated  from  dicoty¬ 
ledons  is  supported  by  evidence  from  gametophytic  development 
and  anatomical  structure  of  seedlings  and  mature  plants,  as  well 
as  by  indications  that  primitive  angiosperms  possessed  a  cambium 
and  were  dicotyledonous,  and  by  the  conclusion  that  the  peculiari¬ 
ties  of  anomalous  dicotyledons  are  secondary.  The  important 
differences  between  monocotyledons  and  anomalous  dicotyledons  on 
the  one  hand,  and  ordinary  dicotyledons  on  the  other,  are  believed 


28 


BOTANICAL  gazette 


[JANUARY 


by  many  to  be  due  to  response  to  the  peculiar  environmental 
conditions  surrounding  the  former. 

14.  Theories  differ  especially  as  to  whether  amphisporangiate, 
entomophilous  flowers  bearing  a  perianth,  or  naked,  anemophilous, 
monosporangiate  ones  are  primitive  among  dicotyledons.  The 
writer  holds,  for  reasons  given,  that  in  the  remote  past  the  ancestors 
of  the  dicotyledons  (and  so  of  all  angiosperms)  possessed  naked, 
unisexual  flowers,  but  that  among  existing  groups  hermaphrodite 
flowers  provided  with  a  perianth  are  primitive,  and  that  the  naked, 
unisexual  forms  existing  today  have  been  secondarily  derived 
from  the  latter;  moreover,  that  the  appearance  of  entomophily, 
the  amphisporangiate  condition,  and  the  perianth  have  been  very 
important  features  in  the  evolution  of  modern  angiosperms. 

15.  The  Bennetti tales,  Gnetales,  and  angiosperms  may  have 
had  common  ancestors  if  we  go  back  to  a  time  prior  to  that  when 
the  Bennettitales  became  a  distinct  line.  It  seems  reasonable  to 
conclude  either  that  angiosperms  were  derived  from  the  same 
ancient  fern  stock  from  which  the  Cycadofilicales  originated,  or 
else  that  they  were  differentiated  from  the  Cycadofilicales  at  a 
very  early  time. 

16.  In  conclusion,  it  is  believed  that  the  most  primitive  of 
existing  angiosperms  are  to  be  found  among  the  Magnoliaceae  or 
related  forms,  and  not  among  forms  with  naked,  monosporangiate, 
anemophilous  flowers. 

Randolph-Macon  College 
Ashland,  Va. 

LITERATURE  CITED 

1.  Andrews,  F.  M.,  Karyokinesis  in  Magnolia  and  Liriodendron  with 
special  reference  to  behavior  of  chromosomes.  Beih.  Bot.  Centralbl. 
n:  134.  1901. 

2.  Arber,  E.  A.  Newell,  and  Parkin,  John,  On  the  origin  of  angio¬ 
sperms.  Jour.  Linn.  Soc.  Bot.  38:  29-80.  1907. 

3.  Brown,  William  H.,  The  nature  of  the  embryo  sac  of  Peperomia.  Bot. 

.  Gaz.  46:  445-460.  1908. 

4.  Campbell,  D.  H.,  Recent  investigations  upon  the  embryo  sac  of  angio¬ 
sperms.  Amer.  Nat.  36:  777-786.  1902. 

5.  Coulter,  J.  M.,  Relation  of  megaspores  to  embryo  sacs  in  angiosperms, 
Bot.  Gaz.  45:361-366.  1908. 


1914] 


M  A  NE  V  A  L—M  A  GNOLIA  CEA  E 


29 


6.  Coulter  and  Chamberlain,  Morphology  of  angiosperms.  1903. 

7.  Coulter  and  Chamberlain,  Morphology  of  gymnosperms.  1910. 

8.  Engler  A.,  in  Engler  and  Prantl’s  Die  natiirliche  Pflanzenfamilien. 
Nachtrag:  Parts  II-IV.  Leipzig.  1897. 

9.  Ernst,  A.,  Ergebnisse  neuerer  Untersuchungen  fiber  den  Embryosack 
der  Angiospermen.  Zurich.  1908. 

10.  Gray,  A.,  Structure  of  the  ovule  and  seed  coats  of  Magnolia.  Jour. 
Linn.  Soc.  Bot.  2: 106.  1857. 

11.  Hallier,  H.,  Ein  zweiter  Entwurf  des  natiirlichen  (phylogenetischen) 
Systems  der  Bliitenpflanzen.  Ber.  Deutsch.  Bot.  Gesells.  23:  85-91.  1905. 

12.  Henslow,  G.,  The  origin  of  monocotyledons  from  dicotyledons,  through 
self-adaptation  to  a  moist  or  aquatic  habitat.  Ann.  Botany  25:  717-744. 
1911. 

13.  - ,  A  theoretical  origin  of  endogens  from  exogens,  through  self¬ 

adaptation  to  an  aquatic  habitat.  Jour.  Linn.  Soc.  Bot,  29:485.  1892. 

14.  Hill,  A.  W.,  Morphology  and  seedling  structure  of  the  geophilous 
species  of  Peperomia.  Ann.  Botany  20:  395-427.  1906. 

15.  Johnson,  D.  S.,  On  the  endosperm  and  embryo  of  Peperomia  pellucida. 
Bot.  Gaz.  30: 1-11.  1900. 

16.  - ,  On  the  development  of  certain  Piperaceae.  Bot.  Gaz.  34:321- 

340.  1902. 

17.  Lignier,  O.,  In  Arber  and  Parkin’s  “The  origin  of  angiosperms.”  1907. 

18.  Mottier,  D.  M.,  Embryo  of  some  anomalous  dicotyledons.  Ann. 
Botany  19:  447-463.  1905. 

19.  Murbeck,  S.,  Parthenogenetische  Embryobildung  in  der  Gattung 
Alchemilla.  Lunds  Univ.  Arsskrift.  36*:  no.  7.  1901. 

20.  Pace,  Lula,  Fertilization  in  Cypripedium.  Bot.  Gaz.  44: 353-374.  1907. 

21.  Parmentier,  Paul,  Histoire  des  Magnoliacees.  Bull.  Sci.  France  et 
Belgique  27:  159-337*  1895. 

22.  Porsch,  Otto,  Versuch  einer  phylogenetischen  Erklarung  des  Embryo- 
sackes  und  der  doppelten  Befruchtung  der  Angiospermen.  1907. 

23.  Queva,  C.,  Contributions  a  l’anatomie  des  monocotyledonees  I.  Les 
Uvulariees  tubereuses.  Lille.  1899. 

24.  Sargant,  Ethel,  Reconstruction  of  a  race  of  primitive  angiosperms. 
Ann.  Botany  22: 121-186.  1908. 

25.  Scott,  D.  H.,  Evolution  of  plants.  1910. 

26.  Senn,  M.  G.,  Die  Grundlagen  des  Hallierischen  Angiospermensystems. 
Beih.  Bot.  Centralbl.  17:  129-156.  1904. 

27.  Smith,  R.  Wilson,  The  tetranucleate  embryo  sac  of  Clintonia.  Bot. 
Gaz.  52:  209-217.  1911. 

28.  Solereder,  Hans,  Systematic  anatomy  of  the  dicotyledons.  Trans,  by 
Boodle  and  Fritsch.  1908. 

29.  Strasburger,  E.,  Die  Samenanlage  von  Drimys  W inter i  und  die  Endo- 
spermbildung  bei  Angiospermen.  Flora  95:  2 15-231.  1905. 


3° 


BOTANICAL  GAZETTE 


[JANUARY 


30.  Thomas,  Ethel  N.,  A  theory  of  the  double  leaf  trace  founded  on  seedling 
structure.  New  Phytol.  6:  77-91.  1907. 

31.  Wettstein,  R.  R.  v.,  Handbuch  der  Systematischen  Botanik.  Vol.  II. 

32.  Wieland,  G.  R.,  American  fossil  cycads.  Washington.  1906.  , 

33.  Worsdell,  W.  C.,  A  study  of  the  vascular  system  in  certain  orders  of 
the  Ranales.  Ann.  Botany  22:  651-682.  1908. 

EXPLANATION  OF  PLATES  I-III 

All  drawings  were  made  with  the  aid  of  a  camera  lucida  from  microtome 
sections. 

Abbreviations  used:  a,  antipodal;  ar,  archesporium;  cb,  cortical  bundle; 
cc,  central  cylinder;  c,  cotyledon;  e,  egg;  em,  embryo;  es ,  endosperm;  fvb, 
fibrovascular  bundle;  ii,  inner  integument;  m,  mechanical  tissue;  mgmc, 
megaspore  mother  cell;  mg,  megaspore;  mcmc ,  microspore  mother  cell; 
mp ,  micropyle;  n,  nucellus;  oi,  outer  integument;  p,  pith;  pc,  parietal  cells; 
ph ,  phloem;  pn,  polar  nucleus;  pt,  pollen  tube;  st,  sporogenous  tissue;  su, 
suspensor;  sy,  synergid;  t,  tapetum;  tc,  tapetal  cell;  te,  tetrad;  v,  vacuole; 
x,  xylem. 

Liriodendron 

Fig.  1. — Part  of  longitudinal  section  of  microsporangium  and  wall; 
wall  somewhat  diagrammatic;  X350. 

Fig.  2. — Pollen  mother  cells  dividing;  X350. 

Fig.  3. — Section  of  pollen  grain  with  reduced  number  of  chromosomes; 
X  600. 

Fig.  4. — Section  of  two-celled  pollen  grain;  X350. 

Fig.  5. — Longitudinal  section  of  young  ovule;  X300. 

Fig.  6. — Megaspore  mother  cell  divided;  X350. 

Fig.  7. — Longitudinal  section  of  ovary  showing  tetrad  of  megaspores 
deeply  buried  within  nucellus;  X350. 

Fig.  8. — Longitudinal  section  of  micropylar  end  of  embryo  sac;  X350. 
Fig.  9. — Polar  nuclei  fusing;  X350. 

Fig.  10. — Longitudinal  section  of  antipodal  end  of  embryo  sac;  X350. 
Fig.  ii. — Transverse  section  of  petiole  showing  arrangement  of  fibro¬ 
vascular  bundles;  X50. 

Fig.  12. — Transverse  section  of  portion  of  central  region  of  diarch  root; 
X590. 

Fig.  13. — Transverse  section  of  hypocotyl;  X50. 

Fig.  14. — Transverse  section  showing  details  of  the  portion  of  fig.  13 
indicated  by  line  ah;  X300. 

Magnolia 

Fig.  15. — Longitudinal  section  of  part  of  apther;  sporogenous  tissue 
differentiated;  X350. 


BOTANICAL  GAZETTE,  LV1I 


PLATE  I 


MANEVAL  on  MAGNOLIACEAE 


) 


BOTANICAL  GAZETTE ,  LV1I 


PLATE  II 


MANEVAL  on  MAGNOLIACEAE 


BOTANICAL  GAZETTE ,  LVII 


PLATE  III 


MANEVAL  on  MAGNOLIACEAE 


1914] 


M  A  NE  V  A  L—M  A  GNOLIA  CEA  E 


31 


Fig.  16. — Longitudinal  section  of  part  of  anther;  microspore  mother 
cells  in  synapsis;  X300.  { 

Fig.  17. — Transverse  section  of  anther;  tapetum  and  sporogenous  tissue 
differentiated ;  X  3  50. 

Fig.  18. — Transverse  section  of  anther;  tetrads  of  microspores;  X300. 

Fig.  19. — Section  of  pollen  grain  with  reduced  number  of  chromosomes; 
X500. 

Fig.  20. — Uninucleate  pollen  grain;  X350. 

Fig.  21. — Binucleate  pollen  grain;  X350. 

Fig.  22. — Longitudinal  section  of  ovule  with  archesporial  cell;  X300. 

Fig.  23. — Longitudinal  section  of  ovule  through  megaspore  mother  cell 
and  tapetal  cell;  X500. 

Fig.  24. — Longitudinal  section  of  ovule;  megaspore  mother  cell;  integu¬ 
ments;  X300. 

Fig.  25. — First  division  of  megaspore  mother  cell;  X350. 

Fig.  26. — Megaspore  mother  cell  divided;  X350. 

Fig.  27. — Tetrad  of  megaspores;  X350. 

Fig.  28. — -Longitudinal  section  through  binucleate  embryo  sac ;  X350. 

Fig.  29. — Longitudinal  section  through  tetranucleate  embryo  sac;  X350. 

Fig.  30. — Longitudinal  section  through  mature  embryo  sac;  X350. 

Fig.  31. — Micropylar  end  of  embryo  sac;  pollen  tube;  two-celled  endo¬ 
sperm;  X600. 

Fig.  32. — Longitudinal  section  of  micropylar  end  of  embryo  sac  showing 
early  condition  of  endosperm;  X300. 

Fig.  33. — Section  of  four-celled  embryo;  X500. 

Fig.  34. — Section  of  eight-celled  embryo;  X500. 

Fig.  35. — Longitudinal  section  through  an  older  embryo;  X500. 

Fig.  36. — Longitudinal  section  of  embryo  and  suspensor;  X300. 

Fig.  37. — Longitudinal  section  of  embryo  from  mature  seed;  X50. 

Fig.  38. — Transverse  section  of  petiole;  X50. 

Fig.  39. — Transverse  section  of  portion  of  a  fibrovascular  bundle  of  a 
petiole;  X300. 

Figv  40. — Transverse  section  of  portion  of  peduncle;  X50. 


. 

-- 


. 

. 

' 

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■ 

w 


. 

■ 


■ 


VITA 


Willis  Edgar  Maneval  was  born  in  Pennsylvania,  on  the  fifth 
day  of  February,  1877.  He  prepared  for  college  at  the  Lycoming 
County  Normal  School,  and  at  Bucknell  Academy,  and  completed 
the  college  course  at  Bucknell  University  in  1902,  receiving  the 
degree  of  Ph.B.,  and  the  following  year  the  degree  of  M.S.  from 
the  same  institution.  He  taught  sciences  in  Bucknell  Academy 
from  1902-6,  and  then  spent  one  year  as  a  graduate  student  at 
the  Johns  Hopkins  University.  From  1907-10  he  was  acting 
professor  of  biology  and  geology  at  Roanoke  College,  Salem,  Vir¬ 
ginia,  after  which  he  returned  to  the  Johns  Hopkins  University  to 
continue  graduate  work,  holding  a  fellowship  in  1911-12.  His 
major  subject  has  been  botany  and  his  subordinates  plant  physi- 
blogy  and  zoology. 


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